The role of threonine in the P2 position of Bowman-Birk proteinase inhibitors: Studies on P2 variation in cyclic peptides encompassing the reactive site loop

Journal of Molecular Biology

Volumn 282, Issue 2, 1998, Pages 447-457

  McBride, Jeffrey D ^a   Brauer, Arnd B E ^a   Nievo, Marco ^a   Leatherbarrow, Robin J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Bowman Birk inhibitor; Canonical loop; Combinatorial chemistry; Proteinase inhibitor; Serine proteinase

Indexed keywords

BOWMAN BIRK INHIBITOR; CHYMOTRYPSIN; CYCLOPEPTIDE; PROTEINASE INHIBITOR; THREONINE;

AMINO ACID SEQUENCE; ARTICLE; ENZYME INHIBITION; HYDROGEN BOND; HYDROLYSIS; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN STRUCTURE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ENERGY METABOLISM; KINETICS; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; BINDING SITES; ENERGY METABOLISM; HYDROLYSIS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES, CYCLIC; THREONINE; TRYPSIN INHIBITOR, BOWMAN-BIRK SOYBEAN;

EID: 0032544235     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2032     Document Type: Article

References (55)

1. Asbóth, B. & Polgár, L. (1983). Transition-state stabilization at the oxyanion binding sites of serine and thiol proteinases: hydrolysis of thiono and oxygen esters. Biochemistry, 22, 117-122.
2. Atherton, E. & Sheppard, R. (1989). Solid Phase Peptide Synthesis, A Practical Approach, IRL Press, Oxford.
3. Bender, M. L., Begué-Canton, M. L., Blakley, R. L., Brobacher, L. J., Feder, J., Gunter, C. R., Kézdy, F. J., Killheffer, J. V., Jr., Marshall, T. H., Miller, C. G., Roeske, R. W. & Stoops, J. K. (1966). The determination of the concentrations of hydrolytic enzyme solutions: α-chymotrypsin, trypsin, papain, elastase, subtilisin and acetylcholinesterase. J. Am. Chem. Soc. 88, 5890-5913.
4. Blow, D. M., Wright, C. S., Kukla, D., Ruehlmann, A., Steigemann, W. & Huber, R. (1972). Model for the association of bovine pancreatic trypsin inhibitor with chymotrypsin and trypsin. J. Mol. Biol. 69, 137-144.
5. Bode, W. & Huber, R. (1992). Natural protein proteinase inhibitors and their interaction with proteinases. Eur. J. Biochem. 204, 433-451.
6. 52 in Cucurbitia maxima trypsin inhibitor-V deduced by trypsincatalyzed hydrolysis and NMR spectroscopy. Biochemistry, 35, 4784-4794.
7. Chen, P., Rose, J., Loves, R., Wei, C. H. & Wang, B. (1992). Reactive sites of an anticarcinogenic Bowman-Birk proteinase inhibitor are similar to other trypsin inhibitors. J. Biol. Chem. 267, 1990-1994.
8. Deslongchamps, P. (1983). Stereoelectronic Effects in Organic Chemistry, Pergamon Press Ltd., Oxford.
9. Domingo, G. J., Leatherbarrow, R. J., Freeman, N., Patel, S. & Weir, M. (1995). Synthesis of a mixture of cyclic peptides based on the Bowman-Birk reactive site loop to screen for serine protease inhibitors. Int. J. Pept. Protein Res. 46, 79-87.
10. Edelhoch, H. (1967). Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry, 6, 1948-1954.
11. Erlanger, B., Kokowsky, N. & Cohen, W. (1961). The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 95, 271-278.
12. Favel, A., Le-Nguyen, D., Coletti-Previero, M. A. & Castro, B. (1989). Active site chemical mutagenesis of Ecballium elaterium trypsin inhibitor II: new microproteins inhibiting elastase and chymotrypsin. Biochem. Biophys. Res. Commun. 162, 79-82.
13. Fersht, A. R. (1974). Catalysis, binding and enzyme-substrate complementarity. Proc. Roy. Soc. ser. B, 187, 397-407.
14. Frigerio, F., Coad, A., Pugliese, L., Lionetti, C., Menegatti, E., Amiconi, G., Schnebli, H. P., Ascenzi, P. & Bolognesi, M. (1992). Crystal and molecular structure of the bovine α-chymotrypsin-eglin c complex at 2.0 Å resolution. J. Mol. Biol. 225, 107-123.
15. Fujinaga, M., Sielecki, A. R., Read, R. J., Ardelt, W., Laskowski, M., Jr. & James, M. N. G. (1987). Crystal and molecular structures of the complex of α-chymotrypsin with its inhibitor turkey ovomucoid third domain at 1.8 Å resolution. J. Mol. Biol. 195, 397-418.
16. Furka, A., Sebestyen, F., Asgedom, M. & Dibo, G. (1991). General method for rapid synthesis of multi-component peptide mixtures. Int. J. Pept. Protein Res. 37, 487-493.
17. Gariani, T. & Leatherbarrow, R. J. (1997). Stability of protease inhibitors based on the Bowman-Birk reactive site loop to hydrolysis by proteases. J. Pept. Res. 49, 467-475.
18. Gronenstein, D. G. & Taira, K. (1984). Stereoelectronic control in peptide bond formation. Ab initio calculations and speculations on the mechanism of action of serine proteases. Biophys. J. 46, 749-761.
19. Heinz, D. W., Priestle, J. P., Rahuel, J., Wilson, K. S. & Grütter, M. G. (1991). Refined crystal structures of subtilisin Novo in complex with wild-type and two mutant eglins. J. Mol. Biol. 217, 353-371.
20. Heinz, D. W., Hyberts, S. G., Peng, J. W., Priestle, J. P., Wagner, G. & Grütter, M. G. (1992). Changing the inhibitory specificity and function of the proteinase inhibitor eglin c by site-directed mutagenesis: functional and structural investigation. Biochemistry, 31, 8755-8766.
21. Ikenaka, T. & Norioka, S. (1986). Bowman-Birk family serine proteinase inhibitors. In Proteinase Inhibitors (Barrett, A. J. & Salvesen, G., eds), pp. 361-374, Elsevier Science Publishers, Amsterdam.
22. Kimura, M., Kouzuma, Y. & Yamasaki, N. (1994). On a Bowman-Birk family proteinase inhibitor from Erythrina variegata seeds. J. Biochem. 115, 369-372.
23. Knorr, R., Trzeciak, A., Bornwarth, W. & Gillessen, D. (1989). New coupling reagents in peptide chemistry. Tetrahedr. Letters, 30, 1927-1930.
24. Lam, K. S., Salmon, S. E., Hersh, E. M., Hruby, V. J., Kazmierski, W. M. & Knapp, J. J. (1991). A new type of synthetic library for identifying ligand-binding activity. Nature, 354, 82-84.
25. Larionova, N. I., Gladysheva, I. P., Tikhonova, T. V. & Kazanskaya, N. F. (1993). Inhibition of cathepsin G and human granulocyte elastase by multiple forms of Bowman-Birk type soybean inhibitor. Biochemistry (Moscow), 58, 1046-1052.
26. Laskowski, M., Jr (1980). An algorithmic approach to sequence → reactivity of proteins. Specificity of protein inhibitors of serine proteases. Biochem. Pharmacol. 29, 2089-2094.
27. Laskowski, M., Jr & Kato, I. (1980). Protein inhibitors of proteinases. Annu. Rev. Biochem. 49, 593-626.
28. Leatherbarrow, R. J. (1990). Using linear and non-linear regression to fit biochemical data. Trends Biochem. Sci. 15, 455-458.
29. Leatherbarrow, R. J. (1992). GraFit (Version 3.0), Erithacus Software Ltd., UK, Staines.
30. Li, Y., Huang, Q., Zhang, S., Liu, S., Chi, C. & Tang, Y. (1994). Studies on an artificial trypsin inhibitor peptide derived from the mung bean trypsin inhibitor: chemical synthesis, refolding, and crystallographic analysis of its complex with trypsin. J. Biochem. (Tokyo), 116, 18-25.
31. Lin, G., Bode, W., Huber, R., Chi, C. & Engh, R. A. (1993). The 0.25-nm X-ray structure of the Bowman-Birk-type inhibitor from mung bean in ternary complex with porcine trypsin. Eur. J. Biochem. 212, 549-555.
32. Longstaff, C., Campbell, A. F. & Fersht, A. R. (1990). Recombinant chymotrypsin inhibitor 2: expression, kinetic analysis of inhibition with α-chymotrypsin and wild-type and mutant subtilisin BPN′, and protein engineering to investigate inhibitory specificity and mechanism. Biochemistry, 29, 7339-7347.
33. 1 cavities of serine proteinases. J. Mol. Biol. 266, 441-461.
34. Maeder, D. L., Sunde, M. & Botes, D. P. (1992). Design and inhibitory properties of synthetic Bowman-Birk loops. Int. J. Pept. Protein Res. 40, 97-102.
35. Markland, W., Ley, A. C., Lee, S. W. & Ladner, R. C. (1996a). Iterative optimization of high-affinity protease inhibitors using phage display. 1. Plasmin. Biochemistry, 35, 8045-8057.
36. Markland, W., Ley, A. C. & Ladner, R. C. (1996b). Iterative optimization of high-affinity protease inhibitors using phage display. 2. Plasma kallikrein and thrombin. Biochemistry, 35, 8058-8067.
37. McBride, J. D., Freeman, N., Domingo, G. J. & Leatherbarrow, R. J. (1996). Selection of chymotrypsin inhibitors from a conformationally constrained combinatorial peptide library. J. Mol. Biol. 259, 819-827.
38. Morhy, L. & Ventura, M. M. (1987). The complete amino acid sequence of the Vigna unguiculata (L) Walp. seed, trypsin and chymotrypsin inhibitor. An. Acad. Brasil Ci. 59, 71-81.
39. Neil, G. L., Niemann, C. & Hein, G. E. (1966). Structural specificity of α-chymotrypsin: polypeptide substrates. Nature, 210, 903-907.
40. Nishino, N., Aoyagi, H., Kato, T. & Izumiya, N. (1977). Studies on the synthesis of proteinase inhibitors. J. Biochem. (Tokyo), 82, 901-909.
41. Odani, S. & Ikenaka, T. (1973). Scission of soybean Bowman-Birk proteinase inhibitor into two small fragments having either trypsin or chymotrypsin inhibitory activity. J. Biochem. 74, 857-860.
42. Pavone, V., Isernia, C., Saviano, M., Falcigno, L., Lombardi, A., Paolillo, L., Pedone, C., Buøen, S., Naess, H. M., Revheim, H. & Eriksen, J. A. (1994). Conformational studies on peptides as enzyme inhibitors: chymotrypsin inhibitors using Bowman-Birk type as models. J. Chem. Soc. Perkin Trans. 2, 1047-1053.
43. Read, R. & James, M. N. G. (1986). Introduction to the proteinase inhibitors: X-ray crystallography. Proteinase Inhibitors (Barrett, A. J. & Salvesen, G. S., eds), pp. 301-335, Elsevier Science Publishers, Amsterdam.
44. Roberts, B. L., Markland, W., Ley, A. C., Kent, R. B., White, D. W., Gutterman, S. K. & Ladner, R. C. (1992). Directed evolution of a protein: selection of potent neutrophil elastase inhibitors displayed on M13 fusion phage. Proc. Natl Acad. Sci. USA, 89, 2429-2433.
45. Schellenberger, V., Braune, K., Hofmann, H.-J. & Jakubke, H.-D. (1991). The specificity of chymotrypsin. Eur. J. Biochem. 199, 623-636.
46. γ. A crystallographic study using peptide cholormethyl ketones as site-specific inhibitors. Biochemistry, 10, 3728-3738.
47. Suzuki, A., Yamane, T., Ashida, T., Norioka, S., Hara, S. & Ikenazka, T. (1993). Crystallographic refinement of Bowman-Birk type protease inhibitor A-II from peanut (Arachis hypogaea) at 2.3 Å resolution. J. Mol. Biol. 234, 722-734.
48. Tam, J. P., Wu, C. R., Liu, W. & Zhang, J. W. (1991). Disulfide bond formation in peptides by dimethyl sulfoxide. Scope and applications. J. Am. Chem. Soc. 113, 6657-6662.
49. Tanaka, A. S., Sampaio, M. U., Marangoni, S., de Oliveira, B., Novello, J. C., Oliva, M. L. V., Fink, E. & Sampaio, C. A. M. (1997). Purification and primary structure determination of a Bowman-Birk trypsin inhibitor from Torresea cearensis seeds. Biol. Chem. 378, 273-281.
50. Terada, S., Sato, K., Kato, T. & Izumiza, N. (1978). Inhibitory properties of nonapeptide loop structures related to reactive sites of soybean Bowman-Birk inhibitor. FEBS Letters, 90, 89-92.
51. Voss, R.-H., Ermler, U., Essen, L.-O., Wenzl, G., Kim, M.-Y. & Flecker, P. (1996). Crystal structure of the bifunctional soybean Bowman-Birk inhibitor at 0.28 nm resolution. Structural peculiarities in a folded conformation. Eur. J. Biochem. 242, 122-131.
52. Wenzel, H. R. & Tschesche, H. (1995). Reversible inhibitors of serine proteinases. In Peptides, Synthesis, Structures, and Applications (Gutte, B., ed.), pp. 321-362, Academic Press, San Diego, CA.
53. Werner, M. H. & Wemmer, D. E. (1992a). Three-dimensional structure of a soybean trypsin/chymotrypsin Bowman-Birk inhibitor in solution. Biochemistry, 31, 999-1010.
54. Werner, M. H. & Wemmer, D. E. (1992b). Identification of a protein-binding surface by differential amide hydrogen-exchange measurements. J. Mol. Biol. 225, 873-889.
55. Zhang, R. G., Lin, G. D., Yan, Y. W., Tang, W. Z., Tan, F. L., Chi, C. W. & Tsao, T. C. (1985). The crystallographic study of the complex of the Lys active fragment of mung bean inhibitor with trypsin. Sci. Sin. 28, 1163-1166.